Parallel evolution of the POQR prolyl oligo peptidase gene conferring plant quantitative disease resistance

Abstract

Plant pathogens with a broad host range are able to infect plant lineages that diverged over 100 million years ago. They exert similar and recurring constraints on the evolution of unrelated plant populations. Plants generally respond with quantitative disease resistance (QDR), a form of immunity relying on complex genetic determinants. In most cases, the molecular determinants of QDR and how they evolve is unknown. Here we identify in Arabidopsis thaliana a gene mediating QDR against Sclerotinia sclerotiorum, agent of the white mold disease, and provide evidence of its convergent evolution in multiple plant species. Using genome wide association mapping in A. thaliana, we associated the gene encoding the POQR prolyl-oligopeptidase with QDR against S. sclerotiorum. Loss of this gene compromised QDR against S. sclerotiorum but not against a bacterial pathogen. Natural diversity analysis associated POQR sequence with QDR. Remarkably, the same amino acid changes occurred after independent duplications of POQR in ancestors of multiple plant species, including A. thaliana and tomato. Genome-scale expression analyses revealed that parallel divergence in gene expression upon S. sclerotiorum infection is a frequent pattern in genes, such as POQR, that duplicated both in A. thaliana and tomato. Our study identifies a previously uncharacterized gene mediating QDR against S. sclerotiorum. It shows that some QDR determinants are conserved in distantly related plants and have emerged through the repeated use of similar genetic polymorphisms at different evolutionary time scales.

Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance

“…For the evaluation of QDR in A. thaliana SALK_077211C ( sop1 ‐2), SALK_058020C ( serk2 ) and SALK_142938C ( snak2 ) 4‐week‐old plants were inoculated with S. sclerotiorum 1980 and lesion size analysed as described in Badet et al . (). The experiment was repeated three times on 7 to 20 distinct plants per genotype.…”

“…Other annotations among the top 1% enriched for predicted S. sclerotiorum sRNA targets included ontologies and domains related to hormone metabolism (GO:0009737 and GO:0046345) and redox metabolism (GO:0055114, GO:0019825 and PF00175). Next, we exploited the probability of association with QDR against S. sclerotiorum for 204 648 single nucleotide polymorphisms (SNPs), obtained through a GWAS in 84 European accessions of A. thaliana (Badet et al, 2017a). We identified 122 034 SNPs distributed in 23 688 gene models, and determined a score of association per gene (-log 10 of the P value for the most significant SNP for each gene).…”

“…Samples for RNA extraction were harvested as described in Badet et al (2017a), separating the centre and periphery of 2.5-mm wide disease lesions with a scalpel blade. For the evaluation of QDR in A. thaliana SALK_077211C (sop1-2), SALK_058020C (serk2) and SALK_142938C (snak2) 4-week-old plants were inoculated with S. sclerotiorum 1980 and lesion size analysed as described in Badet et al (2017a). The experiment was repeated three times on 7 to 20 distinct plants per genotype.…”

“…The expression of A. thaliana Col-0 genes during S. sclerotiorum infection corresponds to expression at the edge of necrotic lesions relative to non-challenged plants, as reported in Badet et al (2017a), data downloaded from the NCBI Gene Expression Omnibus (accession GSE106811). To determine expression of A. thaliana genes during B. cinerea infection, we obtained a dataset from Coolen et al (2016) from the NCBI sequence read archive (https ://www.ncbi.nlm.nih.gov/sra).…”

“…Sclerotinia sclerotiorum is widely dispersed throughout the world and poses a significant threat to agricultural production (Derbyshire and Denton-Giles, 2016). A finished genome for S. sclerotiorum strain 1980 is available (Derbyshire et al, 2017) and GWAS of QDR to S. sclerotiorum in A. thaliana has been reported (Badet et al, 2017a). A previous study has shown that S. sclerotiorum produces sRNAs in vitro (Zhou et al, 2012).…”